Marine diseases have major impacts on ecosystems and economic consequences for aquaculture and fisheries. Understanding origin, spread and risk factors of disease is crucial for management, but data in the ocean are limited compared to the terrestrial environment. Here we investigated how the marine environment drives the spread of viral disease outbreak affecting The Pacific oyster worldwide by using a spatial epidemiology framework. We collected environmental and oyster health data at 46 sites spread over an area of 300 km2 along an inshore-offshore gradient during an epizootic event and conducted risk analysis. We found that disease broke out in the intertidal farming area and spread seaward. Mortalities and virus detection were observed in oysters placed 2 km from the farming areas, but oysters of almost all sites were subclinically infected. Increasing food quantity and quality, growth rate and energy reserves of oyster were associated with a lower risk of mortality offshore whereas increasing turbidity, a proxy of the concentration of suspended particulate matter, and terrestrial inputs, inferred from fatty acid composition of oysters, were associated with a higher risk of mortality. Offshore farming and maintenance of good ecological status of coastal waters are options to limit disease risk in oysters.
Food provisioning influences disease risk and outcome in animal populations in two ways. On the one hand, unrestricted food supply improves the physiological condition of the host and lowers its susceptibility to infectious disease, reflecting a trade-off between immunity and other fitness-related functions. On the other hand, food scarcity limits the resources available to the pathogen and slows the growth and metabolism of the host on which the pathogen depends to proliferate. Here, we investigated how food availability, growth rate and energetic reserves drive the outcome of a viral disease affecting an ecologically relevant model host, the Pacific oyster, Crassostrea gigas. We selected fast-and slow-growing animals, and we exposed them to high and low food rations. We evaluated their energetic reserves, challenged them with a pathogenic virus, monitored daily survival and developed a mortality risk model. Although high food levels and oyster growth were associated with a higher risk of mortality, energy reserves were associated with a lower risk. Food availability acts both as an enabling factor for mortality by increasing oyster growth and as a limiting factor by increasing their energy reserves. This study clarifies how food resources have an impact on susceptibility to disease and indicates how the host's physiological condition could mitigate epidemics. Practically, we suggest that growth should be optimized rather than maximized, considering that trade-offs occur with disease resistance or tolerance.
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